Scientia Horticulturae 138 (2012) 9095

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Scientia Horticulturae
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Role of lenticel morphology, frequency and density on incidence of lenticel

breakdown in Gala apples
S.S. Turketti a , E. Curry b , E. Ltze a,
a
b

Department of Horticultural Science, Stellenbosch University, Private Bag X1, 7602 Matieland, South Africa
Tree Fruit Research Laboratory, U.S. Department of Agriculture, Agricultural Research Service, Wenatchee, WA 98801, United States

a r t i c l e

i n f o

Article history:
Received 16 November 2011
Received in revised form 1 February 2012
Accepted 4 February 2012
Keywords:
Lenticel breakdown
Apples
Royal Gala
Gala sports
Pre-harvest
Microclimate
South Africa

a b s t r a c t
Lenticel breakdown is a skin disorder of apples occurring around the globe. Symptoms of this physiological
disorder can be observed only after harvest. Prevalent on the variety Gala, especially Royal Gala, it is
also observed on the varieties Fuji, Granny Smith, Golden Delicious and Delicious. Lenticel breakdown
is inuenced by a combination of factors that include cultivation and handling practices, however the
causes have not yet been determined. The motivation for the present research was to investigate the
morphology and anatomy of lenticels, evaluating fruits at different stages of development. Fruits were
evaluated from three different orchards in the Western Cape, South Africa, on an attempt to relate physical
and morphological aspects of the fruit to the environment of the different regions. There is an indication
that factors that inuence fruit growth and cuticle development, e.g. relative humidity and temperature,
are directly linked to lenticel breakdown. The lack of lenticel breakdown on the seasons studied limited
our conclusions.
2012 Elsevier B.V. All rights reserved.

1. Introduction
The term lenticel was rst used by Clements (1935) to indicate the white, green, or yellowish-brown spots common on the
surface of apples (Malus domestica Borkh.). In general, lenticels are
small lenticular-shaped openings distributed evenly across the fruit
surface that are formed as the cuticle develops over vestigial stomata during the early stages of fruit development (Clements, 1935;
Curry, 2003). The fruit cuticle is a dynamic tissue, capable of maintaining optimum thickness to accommodate fruit enlargement as
cells within the fruit divide and expand (Curry, 2003, 2005). Under
typical environmental conditions, this cuticle expansion process
occurs gradually by a self-repair mechanism to prevent exposure
of the underlying cells (Curry, 2003).
Lenticels vary in size due to development and position on the
fruit and are more or less open to the atmosphere. The base of
the lenticel is covered with cuticle; however, it is often thinner
than that of surrounding tissue (Curry, 2005). Harker and Ferguson
(1988) recorded that the dimensions and permeability of lenticels
increase during fruit development. They also related lenticel size
with calcium and water uptake in apples (Harker and Ferguson,
1988). Furthermore, they reported an increase in lenticel size late
in the developmental phase associated with cracks and small aws

Corresponding author. Tel.: +27 218083263; fax: +27 218082121.

E-mail addresses: san@sun.ac.za (S.S. Turketti), eric.curry@ars.usda.gov
(E. Curry), elotze@sun.ac.za (E. Ltze).
0304-4238/$ see front matter 2012 Elsevier B.V. All rights reserved.
doi:10.1016/j.scienta.2012.02.010

in the cuticle and concluded that increases and decreases in lenticel

size is a continuing process, therefore agreeing with Currys (2009)
theory of cuticle repair (Harker and Ferguson, 1988).
In apples, the number of lenticels per fruit remains constant for
most of the growing season, while the density declines gradually
as the fruit enlarges (Harker and Ferguson, 1988; Li et al., 2004). In
Starkrimson and Golden Delicious, lenticel density was reported
to be negatively related to anthocyanin accumulation (Li et al.,
2004). According to Clements (1935), the number of lenticels seems
to vary according to variety, for example Delicious has an average
of 803 lenticels per apple, Golden Delicious 843 lenticels Starking Delicious 1313 lenticels and Red Delicious 1379 lenticels. In
addition, within a variety the number of lenticels per apple varies
widely among fruit. In Winesap, the number of lenticels per fruit
was reported to range from 450 to 800 (Clements, 1935), whereas
in Granny Smith, the number per fruit ranged from 655 to 870
(Harker and Ferguson, 1988).
Lenticel breakdown is a skin disorder of apples that manifests
after the fruit have been packed (Curry et al., 2008; Kupferman,
2009a). It appears as a round pit centered on a lenticel and often
occurs on shaded sides or color margins of the fruit. Although
prevalent on Gala apples, especially Royal Gala, lenticel breakdown has also been observed on Fuji, and to a lesser degree on
Granny Smith, Golden Delicious and Delicious (Curry, 2008).
Many factors have been associated with lenticel breakdown and
generally they can be grouped as factors that occur before harvest
and those postharvest. Factors inuencing lenticel breakdown
before harvest include the maturity of the fruit, mineral content

S.S. Turketti et al. / Scientia Horticulturae 138 (2012) 9095

and orchard-specic responses. Although there is an afnity of

certain orchards to consistently have higher levels of lenticel
breakdown, there is a strong year-to-year variation. Among the
factors that occur after harvest, Kupferman (2009b) suggested that
delayed cooling, the use of SmartFresh, of soaps and detergents,
may positively affect lenticel breakdown incidence.
In South Africa, various trials were conducted from 2007/8 to
2010/11 in orchards that showed severe lenticel breakdown during 20042006 (Ltze and Theron, 2009), resulting in up to 50%
loss in Royal Gala exports (personal communication, P. Conradie,
DuToit Agri). These trials evaluated the inuence of most aspects
cited in literature known to inuence lenticel breakdown incidence.
In spite of extensive research the past few years, results regarding
the initiation or cause of lenticel breakdown in Royal Gala were not
conclusive mainly due to lack of lenticel breakdown manifestation.
The present paper describes a new etiological approach: (1) a histological study of lenticel size on fruit at 40, 70 and 100 (commercial
harvest) days after full bloom (dafb) and its relationship with early
season temperatures and (2) correlation of lenticel density with
lenticel breakdown development; with the presuppose that lenticel breakdown incidence could be related to microclimate and fruit
development.

2. Materials and methods

2.1. Lenticel distribution and size in Western Cape, South Africa
2.1.1. Using peel imprints to determine number and size of
lenticels per cm2
Royal Gala apple fruits were sampled from three different
orchards in the Ceres area, Western Cape, South Africa, according to previous lenticel breakdown occurrences. In Tandfontein
(TFT 32 46 32.76S, 19 14 25.86E) where lenticel breakdown
was previously indicated as severe, Vastrap (VAS 33 15 10.40S,
19 14 33.22E) where lenticel breakdown was previously indicated
as moderate and Nooitgedaght (NGD 33 12 35.45S, 19 19 50.24E)
where lenticel breakdown was not present. Trees were all planted
on M793 rootstock and managed according to commercial practices. Fruit were harvested at 40, 70 and 100 dafb (commercial
harvest), comprising three treatments and three phenological
phases of fruit development. Ten fruit of similar size were randomly selected from each site and each phenological stage. Prints
were made from 1 cm2 peel sections of the fruit on the median
part, from the green (inside) and red (outside) sides of each fruit.
The two sides were identied to address the possible inuence of
heat and light exposure on lenticels number and size. The material
was prepared according to Wilson et al. (1981). Each imprint was
then observed under a light microscope (Nikon Eclipse E 600, Nikon
Instruments Europe B.V., Amstelveen, Netherlands) under 10 or 20
times magnication, to determine the number of lenticels per cm2 .
Digital micrographs were taken of three lenticels per side per fruit
(Nikon Digital Camera, DXM 1200C) and used to measure the width
and length of each lenticel. The measurements were made with the
use of NIS Elements D 2.3 Program (Nikon Instruments). Mass and
diameter were also recorded for each apple.

2.1.2. Measuring length and depth of lenticels by cross-sections

From the samples described above, 6 fruits were selected
randomly for microscopy studies. Lenticel cross-sections were
hand-made of three lenticels from both sides of the fruit (green
and red), placed on a microscope slide in a drop of water, covered
with slips and observed under a light microscope (Nikon Eclipse E
600) (Fig. 1). Digital micrographs were taken (Nikon Digital Camera, DXM 1200C) and used to measure the depth and length of

91

Fig. 1. Cross-section of a lenticel used for anatomical measurements of A: length

and B: depth. Bar is 100 m.

each lenticel. The measurements were made with the use of NIS
Elements D 2.3 Program (Nikon Instruments).
2.1.3. Lenticel development stages
Based on size and appearance, lenticels were classied according to stages of development as immature, intermediate and
developed.
2.2. Collection of temperature data
Hourly temperatures were collected from 2004/5, when the
rst severe lenticel breakdown incidence was reported at TFT to
2010/11, using automatic weather stations. During 2009/10 to
2010/11, similar data for NGD and VAS also became available.
2.3. Statistical analysis
Data were analyzed statistically using the PROC GLM procedure
from the Statistical Analysis System (SAS) program (SAS Institute
Inc., 2004, Cary, NC). Results were considered signicantly different
using the LSD of 5%.
2.4. Lenticel density and lenticel breakdown in Gala sports in
Washington State, USA
A preliminary study was initiated in 2009 in an experimental
orchard of 9-year-oldGala sports on Malling 26 rootstock growing
in sandy loam near Orondo, WA (47 33 54.33 N, 120 14 32.23 W;
elevation 289 m). Gala sports included, Brookeld, Pacic,
Royal and UltraRed and were planted in a completely randomized block design of three replications of seven trees. Although fruit
set was generally heavy, hand thinning in late spring reduced crop
load to a moderate level. Trees were irrigated by undertree impact
sprinklers.
Fruit esh rmness and starch clearing were evaluated using
standard methods every 57 days beginning about 20 days before
anticipated harvest. To allow for maximum growth, fruit were harvested when the starch was 8090% converted, at which time 10
apples of approximately the same diameter were removed from
the east side of each of three middle trees per replication (n = 90).
Fruit were taken to the laboratory and stored at 1.1 C until further examination. Individual fruit were weighed and the number
of lenticels on each apple at the widest part was counted within a
20 mm diameter ring on opposite sides of the fruit, perpendicular to
the most exposed side. Lenticel density was calculated by dividing
the number of lenticels by the area within the ring and averaging

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S.S. Turketti et al. / Scientia Horticulturae 138 (2012) 9095

Table 1
Sampling dates for 2009/10 and 2010/11 for the three different sites.
Phenological phase

Vastrap (VAS)

40 dafb
70 dafb
100 dafb

23/11/09
22/12/09
27/01/10

Tandfontein (TFT)
01/12/10
05/01/11
11/02/11

this calculation from both sides. Fruit was returned to cold storage
at 1.1 C for about ve months.
After 150 days at 1.1 C, apples were processed over a smallscale packing line to induce lenticel breakdown similar to the
method described previously (Curry et al., 2008) with minor modications. First, cold fruit were submerged for 3 min in a water bath
kept at 33 C, after which they were placed on the packing line and
conveyed through a soap wash, cool water rinse, wax treatment,
brush polisher and warm air (43.3 C) dryer. Apples were placed
on trays in boxes and returned to 1 C for 48 h before recording lenticel breakdown values. Lenticel breakdown was assessed by
counting the number of discrete, darkened, lenticel-centered pits
within a 2 cm diameter ring placed over the most severely affected
area of the fruit. Data are presented as the percentage of fruit with
lenticel breakdown values >1.
3. Results
3.1. Lenticel distribution and size in Western Cape, South Africa
3.1.1. Using peel imprints to determine number and size of
lenticels per cm2
Sampling dates for the three phenological stages for each site
during the two seasons are summarized in Table 1. For each of the
dates, the average number of lenticels on 1 cm2 of an apple (on the
median part of two opposite sides of six apples) was counted and
results are presented in Table 2. The developmental stage of the
lenticel was also recorded (Table 2).
The number of lenticels analyzed through imprints made from
apple skins, show a similar pattern of that found in literature,
averaging from 2 to 10 on 1 cm2 . The average number of lenticels
at harvest on 1 cm2 for all sites during 2010/11 (4.3) was almost
50% lower than that calculated in 2009/10 (8.3). The average fruit
size of the crop was smaller in 2010/11 compared to the previous
season for all three sites, and is unfortunately not available for the
fruit used for the actual lenticel measurements. If the average fruit
diameter of the sites is accepted as representative of the sampled
fruit, the hypothetical fruit surface area for each site could be calculated and from that, the hypothetical number of lenticels per fruit
calculated for each site at harvest. This indicated that, not only was
the fruit smaller during 2010/11, but this lead to substantially less
lenticels per fruit, given the assumptions for the calculations, which
is contrary to the principle that lenticel number per cm2 decreases
as fruit size increases when fruit expands. At harvest, fruits from
the 2010 season had approximately half the number of lenticels
compared to fruit from 2009. However these fewer lenticels in 2010
were larger in size and further developed than the lenticels of 2009.
This may have enabled the fruit to respond similarly under comparable conditions, regarding moisture loss through the lenticels.
During both seasons, TFT had signicantly more lenticels per
cm2 compared to the other two sites at 40 dafb. This trend continued at 70 dafb during 2009/10, but no signicant differences were
observed between the sites in 2010/11. Similarly, the signicant
differences between TFT and the other sites continued until harvest 2009/10, but again, this was not found for lenticel numbers
at harvest 2010/11. TFT showed a signicantly higher number of
lenticels per fruit compared to the other two sites during 2009/10
and at 40 dafb in 2010/11. The higher number of lenticels found

23/11/09
22/12/09
27/01/10

Nooitgedaght (NGD)
14/12/10
05/01/11
4/03/11

25/11/09
22/12/09
27/01/10

10/12/10
05/01/11
17/02/11

in TFT could be related to climatic conditions at this site. During

November 2009/10 and 2010/11 (approx. 1545 dafb), TFT maximum temperatures were higher than those of VAS, which could
have predisposed the formation of a higher number of lenticels.
According to Curry (2003), climacteric conditions inuence the
rate of fruit expansion and wax development. If rapid climate
changes from cool, cloudy conditions to hot, dry, sunny conditions
occur, e.g. at microclimate conditions in an orchard or different
experimental sites, wax development may be delayed because of
either the inuence of excessive incident radiation-induced heat
stress, or the inability of the fruit to supply sufcient substrate
for wax development. Under these conditions, the underlying cells
may become exposed to the desiccation pressure of the environment and start to produce suberin along the exposed cell surfaces,
leading to openings that may appear as ne white cracks. If these
climatic conditions remain for an extended period, lenticels are
forced to expand and the cuticle may also crack and expose the
unprotected cells beneath the cuticle. Between 70 and 100 dafb,
the nal phase of fruit expansion, the cuticle almost doubles in size.
During this phase in 2010/11 season (data not shown), TFT had an
increase in relative humidity and the temperature remained constant. It is possible that these conditions favored cuticle formation

Table 2
Average number of lenticels per cm2 from two opposite sides of a Royal Gala apple
(median) on three different sampling dates (40 dafb, 70 dafb and 100 dafb-harvest)
for 2009/10 and 2010/11 seasons. Stage represents the mean developmental phase
of the lenticels, averaged across replicated samples per date. Different letters within
orchards indicate statistically signicant differences on a 5% level.
Treatment

40 dafb
2009/10

2010/11
2

Lenticels (cm )

Stage

Lenticels (cm2 )

Stage

NGD
VAS
TFT

9.33a
5.42a
27.80b

1.5 ns
1.2
1.2

12.17a
9.92a
21.58b

1.0a
1.0
1.0

LSD5%
P>F

9.24
<0.0001

0.3734
0.5654

Treatment

70 dafb
2009/10

2010/11
2

NGD
VAS
TFT
LSD5%
P>F
Treatment

Lenticels (cm )

Stage

Lenticels (cm2 )

Stage

7.42a
7.17a
16.08b

1.5 ns
2.0
1.2

8.83 ns
6.67
8.91

1.3ab
2.2a
1.2b

0.1156
0.7996

4.331
0.4951

0.0497
0.8407

4.28
0.0002
Harvest
2009/10

2010/11
2

NGD
VAS
TFT
LSD5%
P>F
a

6.208
0.0013

Lenticels (cm )

Stage

Lenticels (cm2 )

Stage

7.08a
6.42a
11.33b

2.5 ns
2.7
2.7

4.08 ns
4.67
4.42

1.7b
2.8a
1.7b

0.8746
0.7890

4.227
0.9611

0.0057
0.7452

3.82
0.0269

No statistical analysis was performed because stages were similar.

S.S. Turketti et al. / Scientia Horticulturae 138 (2012) 9095

Table 3
Average length and depth of lenticels from two opposite sides of Royal Gala apples
as determined with a cross-section of a lenticel on three different sampling dates
(40 dafb, 70 dafb and 100 dafb-harvest) for 2009/10 and 2010/11 seasons. Different
letters within orchards indicate statistically signicant differences on a 5% level.
Treatment

40 dafb
2009/10

2010/11

Length

Depth

Length

Depth

NGD
VAS
TFT

337.65b
440.78a
477.54a

114.44c
194.73a
164.04b

610.26 ns
724.33
655.33

171.75 ns
222.82
199.85

P
LSD5%

0.0288
102.62

0.2714
133.12

0.0277
35.96

Treatment

<0.0001
27.377

70 dafb
2009/10

NGD
VAS
TFT
P
LSD5%
Treatment

2010/11

Length

Depth

Length

Depth

575.81a
415.39c
527.88b

166.84b
203.08a
166.33b

654.52 ns
757.11
707.56

218.02 ns
217.85
203.14

0.3354
142.61

0.5714
33.78

<0.0001
41.497

<0.0001
20.963

Harvest
2009/10

2010/11

Length

Depth

Length

Depth

NGD
VAS
TFT

532.77b
770.89a
617.06b

181.44c
253.49a
218.13b

1091.52a
667.01b
1168.22a

242.41b
181.25a
293.59b

P
LSD5%

0.0007
104.08

0.0018
34.512

<0.0001
183.69

0.0046
60.401

and wax development and therefore the masking of some lenticels

due to a slower fruit growth rate (Curry, 2005). Based on previous
studies (Curry, 2003, 2005, 2009; Tessmer, 2009) and observations
in the present study, it seemed possible that immature lenticels
(stomata) at 40 dafb can eventually be covered by the cuticle, resulting in a lower lenticel number at harvest.
3.1.2. Measuring length and depth of lenticels by cross-sections
Table 3 shows the average size in depth and length of a typical
lenticel at the three phenological stages, for both seasons. At 40
dafb, the length of the lenticels in NGD was signicantly smaller
than the other two sites length in 2009/10, but the depth of the
lenticels were all signicantly different from one another. At 70
dafb in 2009/10, the lengths of lenticels in all three sites differed
signicantly from one another and the depth of lenticels in VAS
was signicantly bigger than the other sites. At harvest in 2009/10,
the length and depth of the lenticels from VAS were signicantly
bigger that for the other sites. The lenticel depth varied significantly between all three sites, with the shallowest in NGD and
deepest in VAS. During the following season, no signicant differences between sites were noted at 40 and 70 dafb. At harvest, the
lenticel length and depth in VAS were signicantly smaller that for
the other two sites, but the lenticel depth all differed between sites,
with the smallest in VAS and deepest in TFT.
When the size of lenticels was determined through crosssections, air pockets were observed underneath openings in the
epidermis. This was noticed mainly at 40 dafb in immature and
intermediate lenticels. Partial separation of the lenticels from the
surrounding epidermis has been observed previously in Elstar,
Falstaff, Gala, Galaxy, Golden Delicious and Pinova apples
(Amiri and Bompeix, 2005; Tessmer, 2009). This phenomenon can

93

be aggravated by a sudden abundant water supply after a period of

drought (Curry, 2003).
3.1.3. Lenticel development stages
During 2009/10, there were no signicant differences between
the sites during the three phenological stages (Table 2). However,
there was a shift from a dominant immature phase (1) at 40
dafb towards a developed stage (3) at harvest. Similarly, during
2010/11, no signicant differences between sites were found at 40
dafb, with a dominant immature phase. However, at 70 dafb, the
developmental stage at VAS was signicantly different from that of
TFT, but not from NGD. While VAS showed more cells in the intermediate stage (2), the other two sites tended to have immature
(1) cells. At harvest, the signicant difference between the developmental stages of VAS (2.8) and TFT (1.7) remained, with NGD
(1.7) also differing signicantly from VAS. At harvest 2010/11, the
general stage of development (1.72.8) also lagged behind that of
2009/10 (2.52.7).
Although all three stages of lenticel development, as dened
in our study, occurred on the fruit surface throughout the different
developmental fruit phases, immature lenticels occurred in higher
numbers during the rst phase of fruit development (40 dafb) and
were more difcult to observe during the subsequent fruit developmental phases. The developed stage was rarely found in the
beginning of fruit development, but became more abundant after
the fruit reached its nal size (70 dafb onwards).
3.2. Temperature data
From the temperature data, growing degree hours during fruit
development were calculated for TFT and VAS, from full bloom
to rst harvest (data not shown). NGD temperatures were only
available for 2010/11. No obvious trends could be found that could
describe the lenticel breakdown sensitive seasons. Maximum daily
temperatures during January and February (data not shown) could
also not be related to the lenticel breakdown incidence reported in
2004/5, 2005/6 (high lenticel breakdown) or 2006/7 (some lenticel
breakdown incidence).
We also examined daily maximum temperature early during the
season, dividing the season into 20 days intervals from full bloom
until 70 dafb. From approx. 27 to 41 dafb during 2004 and 2005
(high lenticel breakdown), maximum hourly temperatures at TFT
seemed to be consistently higher than during the years of no or little
lenticel breakdown e.g. 2007 and 2009 (Fig. 2). Although no lenticel
breakdown was found in the samples in either 2009/10 or 2010/11,
temperatures during 2008 followed a similar trend to those of 2004
and 2005 (data not shown). Fig. 3 shows the temperatures above
20 C between approx. 15 and 45 dafb for both seasons and indicates
higher temperatures occurring at TFT compared to VAS. This may
partly explain the higher number of lenticels found at 40 dafb for
both seasons in TFT compared to VAS. In Fig. 4, the number of days
with a relative humidity lower than 40% (stress conditions), shows
data only for TFT, indicating that these conditions did not occur at
VAS during December 2009/102010/11, corresponding to 4070
dafb.
3.3. Lenticel density and lenticel breakdown in Gala sports in
Washington State, USA
There was no difference in fruit maturity among the four Gala
sports according to measurements of starch clearing index and fruit
esh rmness (data not shown). On the other hand, there were
differences among sports of both lenticel density and lenticel breakdown. There was a highly correlated inverse relationship (Pearson
correlation coefcient = 0.91) between lenticel and percent lenticel breakdown (Fig. 5). Brookeld had the lowest lenticel density

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S.S. Turketti et al. / Scientia Horticulturae 138 (2012) 9095

30
25
04TFT

20

05TFT
06TFT

15

41

34

27

10

20

08TFT

Days after full bloom

A
Temperature (C)

35

5
Correlaon coecient = 0.91

30

20

10

30
25
04TFT

20

07TFT
09TFT

15

41

34

20

27

10TFT

10

Fig. 5. Lenticel breakdown () and lenticel density () on different Gala sports of
similar fruit diameter grown near Orondo, Washington in 2009. Lenticel breakdown
is shown as the percent of apples with more than two lenticel breakdown pits,
whereas lenticel density is the number of lenticels per cm2 peel surface area. Bars
indicate + SE.

Day after full bloom

Fig. 2. Average maximum hourly temperatures from 20 to 47 dafb for the Tandfontein (TFT) weather station from 2004 (04TFT) to 2010 (07TFT, 09TFT, 10TFT).
(A) Years with lenticel breakdown incidence (2004, 2005, 2006) versus no lenticel
breakdown (2008) and (B) lenticel breakdown (2004) versus no lenticel breakdown
(2007, 2009, 2010).

09TFT

Temperature in C

Lencel breakdown (% incidence)

40

Lencel density (number cm2)

Temperature (C)

35

34

10TFT

32

09VAS
10VAS

30
28
26
24

and highest percent lenticel breakdown, whereas the reverse was

true for UltraRed.
Pooled data indicated no signicant correlation between lenticel
density and fruit weight (Fig. 6). However, correlation coefcients
for Brookeld, Pacic, Royal and UltraRed were 0.42, 0.13,
0.13, and 0.24, respectively. That is, the direction of correlations, i.e., the correlation moments, varied from positive to negative
with increasing lenticel density. Although this is a preliminary nding and correlation coefcients are weak, data may indicate that
Gala sports with a higher propensity for developing lenticel breakdown show increased incidence as fruit weight (size) increases,
whereas sports with a lower propensity to develop lenticel breakdown do not. This may indicate susceptible fruit are less able to
repair cracking of the lenticular annulus. Further research is needed
to substantiate this possibility.

22
20
1

15

22

30

Fig. 3. Temperatures above 20 C for November that corresponds to approximately

1545 dafb for the two sites (TFT and VAS) for 2009/10 (09) and 2010/11 (10).

40

Relative Humidity (%)

35
30
25
20
15

09TFT

10

10TFT

09VAS
10VAS

0
31

38

45

52

60

December
Fig. 4. Relative humidity below 40% for December that corresponds to approximately 3565 dafb for the two sites (TFT and VAS) for 2009/10 (09) and 2010/11
(10).

Lencel density (number cm2)

November

Correlaon coecient = -0.04

1
180

200

220

240

260

280

Fruit weight (g)

Fig. 6. Lenticel density as a function of fruit weight for all Gala sports sampled from
Washington in 2009. Straight line indicates direction of the correlation coefcient
whereas ellipse is centered on the sample means of the x and y variables (P < 0.95).

S.S. Turketti et al. / Scientia Horticulturae 138 (2012) 9095

4. Discussion
Lenticel breakdown has been associated with a variety of factors
that range from pre-harvest cultural practices to storage management, including ambient conditions. This study examined the
possibility that lenticel breakdown might be related to Gala strain,
lenticel size and phenological stage. Results from Ceres revealed
that environmentally different cultivation sites presented fruit with
signicant differences in number of lenticels. The highest incidence
of lenticel breakdown was reported in Tandfontein after a year
(2004/05) where the average maximum temperatures throughout
the year were extreme compared to the other sites.
Although no lenticel breakdown was observed during the two
seasons investigated, Tandfontein had a higher number of lenticels
of larger sizes. Relative humidity at Tandfontein and Nooitgedaght
was lower (Ave.: 52.0%) in comparison to Vastrap (Ave.: 77.1%) from
full bloom to harvest during the two evaluation seasons and was followed by a constant number and size of lenticels. We believe that
climate information, such as temperature and relative humidity,
are important observations during fruit development as indicators
for post-harvest management, and can enable early predictions of
possible lenticel breakdown allowing for preventative measurements.
The evaluation of lenticel size, including imprints and crosssections, did not present any distinct pattern and therefore we
could not establish a relationship between lenticel size and lenticel breakdown incidence. In contrast, the developmental stage of
the lenticels revealed a distinct pattern that followed the fruit
developmental stages. While some authors denominate the immature lenticels as stomata, maintaining the principle proposed by
Clements (1935), we described a lenticel as any opening in the cuticle providing it has the shape of the stomata or resembles a crack in
the cuticle. In addition, our analysis indentied air pockets underneath the lenticel regions that may contribute to the occurrence
of lenticel breakdown in apples. How the air pockets originate
and their possible inuence in lenticel breakdown still needs to
be conrmed.
From the study in Washington State, a highly correlated inverse
relationship between lenticel and percent lenticel breakdown was
established. No signicant correlation between lenticel density and
fruit weight was found. This may indicate susceptible fruit are less
able to repair cracking of the lenticular annulus. Further research
is needed to substantiate this possibility.
5. Conclusion
The study of lenticel morphology indicated that relative
humidity and temperature can play an important role in lenticel
breakdown due to their inuence on the rate of fruit growth
and cuticle development, both related to fruit development.
Environmental conditions at fruit development should be taken
into consideration when planning for future studies. Factors that

95

inuence cuticle development, mainly at the nal stages of fruit

growth, should also be investigated. Finally, these studies should
be repeated often in orchards where lenticel breakdown incidence
is consistent to substantiate conclusions. Climate change predictions in the Cape Floristic Region of South Africa involve 0.51.0 C
increase in temperature and 25% decrease in annual rainfall
(Rutherford et al., 1999). This will result in wider variations of
temperature and humidity than observed nowadays and therefore
a higher incidence of skin disorders.
Acknowledgements
In South Africa, we wish to thank Mrs. P. Conradie and DuToit
Agri for supplying the fruit and historical information in Ceres, as
well as Fruitgro Services and the National Research Foundation who
funded the research.
References
Amiri, A., Bompeix, G., 2005. Diversity and population dynamics of Penicillium spp.
on apples in pre- and postharvest environments: consequences for decay development. Plant Pathol. 54, 7481.
Clements, H.F., 1935. Morphology and physiology of pome lenticels of Pyrus malus.
Bot. Gaz. 97 (1), 101117.
Curry, E.A., 2003. Factors associated with apple lenticel breakdown. In: Postharvest
Information Network., http://postharvest.tfrec.wsu.edu/REP2003B.pdf.
Curry, E.A., 2005. Ultrastructure of epicuticular wax aggregates during fruit development in apple (Malus domestica Borkh.). J. Hortic. Sci. Biotechnol. 80 (6),
668676.
Curry, E.A., 2008. Effects of 1-MCP applied postharvest on epicuticular wax of
apples (Malus domestica Borkh.) during storage. J. Sci. Food Agric. 88 (February),
9961006.
Curry, E.A.,2009. Growth-induced microcracking and repair mechanisms of fruit
cuticles. In: Proceedings of the SEM Annual Conference. Society for Experimental Mechanics Inc., Albuquerque, NM, USA, http://sem-proceedings.com/09s/
sem.org-SEM-2009-Ann-Conf-s078p04-Growth-induced-MicrocrackingRepair-Mechanisms-Fruit-Cuticles.pdf.
Curry, E.A., Torres, C., Neubauer, L., 2008. Preharvest lipophilic coatings reduce lenticel breakdown disorder in Gala apples. Horttechnology 18 (4), 690696.
Harker, F.R., Ferguson, I.B., 1988. Transport of calcium across cuticles isolated from
apple fruit. Sci. Hortic. 36, 205217.
Kupferman, E., 2009a. Lenticel breakdown in Gala apples, 2008 crop. In: Postharvest
Information Network., http://postharvest.tfrec.wsu.edu/EMK2009C.
Kupferman, E., 2009b. Plain talk about apple lenticel breakdown. In:
Postharvest
Information
Network.,
http://postharvest.tfrec.wsu.edu/
EMK2007C.pdf.
Li, X.J., Hou, J.H., Zhang, G.L., Liu, R.S., Yang, Y.G., Hu, Y.X., Lin, J.X., 2004. Comparison of anthocyanin accumulation and morpho-anatomical features in apple skin
during color formation at two habitats. Sci. Hortic. 99, 4153.
Ltze, E., Theron, K.I., 2009. Investigation of factors contributing to the development
of lenticels breakdown in Royal Gala apples in South Africa. In: ASHS 2009
Annual Conference, St. Louis, MO, USA, August 2429, 2009.
Rutherford, M.C., Midgley, G.F., Bond, W.J., Powrie, L.W., Roberts, R., Allsopp, J., 1999.
South African country study on climate change: plant biodiversity, vulnerability and adaptation assessment. In: Final Report. US Country Study on Climate
Change.
Tessmer, M.A., 2009. Anatomical and physico-chemical characteristics of fruits of
apple trees (Malus domestica Borkh.) and their relations to lenticel breakdown.
Doctoral Dissertation: 75. Escola Superior de Agricultura Luiz de Queiroz, Universidade de So Paulo, So Paulo, BR.
Wilson, C.L., Pusey, P.L., Otto, B.E., 1981. Plant epidermal sections and imprints using
cyanoacrylate adhesives. Can. J. Plant Sci. 61, 781783.